Anopheles gambiae M and S are thought to be undergoing ecological speciation by adapting to different larval habitats. Toward an improved understanding of the genetic determinants and evolutionary processes shaping their divergence, we used a 400,000 single-nucleotide polymorphism (SNP) genotyping array to characterize patterns of genomic differentiation between four geographically paired M and S population samples from West and Central Africa. In keeping with recent studies based on more limited genomic or geographic sampling, divergence was not confined to a few isolated "speciation islands." Divergence was both widespread across the genome and heterogeneous. Moreover, we find consistent patterns of genomic divergence across sampling sites and mutually exclusive clustering of M and S populations using genetic distances based on all 400,000 SNPs, implying that M and S are evolving collectively across the study area. Nevertheless, the clustering of local M and S populations using genetic distances based on SNPs from genomic regions of low differentiation is consistent with recent gene flow and introgression. To account for these data and reconcile apparent paradoxes in reported patterns of M-S genomic divergence and hybridization, we propose that extrinsic ecologically based postmating barriers vary in strength as environmental conditions fluctuate or change.